Exposure to known and emerging groundwater contaminants significantly alters poultry microbiome and metabolome

The exposome represents a summation of exposures which influence an individual’s health over their lifetime. Understanding the exposome will aid in determining the environmental factors that contribute to disease states. Due to the biological complexity of the exposome and the resulting high dimensionality of the data, it is relatively difficult to predict adverse health outcomes resulting from a summation of environmental exposures. Therefore, accurate and relevant exposome criteria for biological assays is the first step toward addressing the current knowledge gaps for exposome research. This study aims to assess the presence of and health effects from exposure to contaminants in Wisconsin groundwater. We focused on three co-occurring chemicals that were detected at concentrations exceeding groundwater standards (i.e., nitrate, atrazine and imidacloprid) and the emerging contaminant, microplastics (i.e., polyethylene fiber). The agricultural chemical mixture of nitrate, atrazine and imidacloprid represent a known and ecologically relevant contaminant because each chemical individually has health risk levels established. Microplastics (MPs) are plastic fragments less than 5 mm in diameter that have been implicated in intestinal toxicity, altered metabolites, and other adverse health outcomes following exposure. In recent years, MPs have increasingly been found in locations where there could be interaction with other environmental contaminants such as pesticides. However, there is limited knowledge regarding the impacts of MPs on health of terrestrial species sources such as poultry. In this study, broilers were exposed to two ternary chemical mixtures or polyethylene microplastics (PE MPs) for 49 days. We observed significant perturbations to the cecal microbiome and metabolome of broiler in all exposure groups. We observed that both ternary mixtures and PE fiber MPs significantly altered the cecal microbiomes as determined by the enrichment of genera, Fournierella, Ruminococcus and an unclassified genus in the family Coriobacteriaceae. Perturbations to cecal microbial activity were also confirmed via modulation of pathways such as the pentose phosphate pathway, Vitamin B metabolism and metabolism of xenobiotics by cytochrome P450. The data presented here will aid in improving current groundwater regulations for agricultural chemical mixtures and microplastics.

暴露组(Exposome)指个体在整个生命周期中所有影响其健康的暴露因素的总和。明确暴露组的构成，有助于解析引发疾病状态的环境驱动因素。由于暴露组本身具有生物学复杂性，且对应数据集存在高维特性，基于环境暴露的综合效应预测不良健康结局的难度相对较高。因此，适配生物学实验的精准且贴合实际的暴露组判定标准，是填补当前暴露组研究领域知识空白的首要环节。本研究旨在评估威斯康星州地下水中污染物的暴露情况及其对健康的影响。本研究聚焦于三类浓度超出地下水安全标准的共现化学物质（即硝酸盐、莠去津与吡虫啉），以及新兴污染物微塑料(MPs，即聚乙烯纤维)。由硝酸盐、莠去津与吡虫啉组成的农药混合物属于已知且具备生态学相关性的污染物，因为单种化学物质均已确立明确的健康风险等级。微塑料(MPs)指直径小于5毫米的塑料碎片，已有研究证实其暴露后可引发肠道毒性、代谢谱改变及其他不良健康结局。近年来，在可与农药等其他环境污染物发生交互作用的区域，微塑料的检出率持续攀升，但目前关于微塑料对家禽等陆生生物健康的影响，相关研究与认知仍较为有限。本研究中将肉鸡暴露于两种三元化学混合物或聚乙烯纤维微塑料(PE MPs)中，暴露时长为49天。我们观察到，所有暴露组的肉鸡盲肠微生物组(cecal microbiome)与代谢组(metabolome)均出现显著扰动。通过菌属丰度变化分析（弗尼氏菌属Fournierella、瘤胃球菌属Ruminococcus以及棒杆菌科Coriobacteriaceae下的未分类菌属）证实，三元化学混合物与聚乙烯纤维微塑料均显著改变了肉鸡的盲肠微生物组结构。磷酸戊糖途径、维生素B代谢以及细胞色素P450对外源物质的代谢等通路的调控变化，也进一步证实了盲肠微生物活性的扰动。本研究提供的实验数据，将有助于完善当前针对农药混合物与微塑料的地下水监管规范。